Sunday, February 23, 2014

Our understanding and expectations of how natural selection
should lead to adaptive evolution in the wild is heavily informed by predictions
derived from theoretical and laboratory studies. These, although useful in
expanding our understanding of evolutionary processes, tend to consider only a
single source of selection, and thus do not encompass the complexity of natural
environments where multiple sources of selection interact simultaneously. Field
surveys, on the other hand, do integrate the complexity of nature, but are
limited in their ability to disentangle cause and effect. As a result, field
studies often do match our predictions – but sometimes our predictions totally
miss the mark, and it is difficult to figure out why. A way of bridging these
two approaches is to experimentally manipulate an environmental factor of
interest in nature, allowing cause and effect to be connected even in a complex
system.

Evidence that drastic changes in an organism’s environment can
lead to rapid adaptive evolution has proliferated in the past 20 years.These drastic
changes come in many forms and flavours, but they generally involve the emergence –
or, less frequently, the loss – of a selective factor. Several studies in the
wild report that introducing new predators, contaminants, competitors, or
parasites can lead to an increase in the ability of the affected populations to
deal with the new stressors; the population adapts to the new source of
selection. We commonly assume that the reverse should also be true: the loss of
a source of selection (i.e. relaxed selection) should lead to the loss of the
ability to deal with that stressor. However, there is good evidence suggesting
that traits might not change for relatively long periods of time after the loss
of a source of selection (see Lahti
et al. 2009), perhaps because change might be driven only by drift, if the
cost of the adaptation to the stressor was very low.

Through a series of field introductions in collaboration
with the FIBR Guppy Project we tested
whether removing Gyrodactylus spp., a
common and deleterious ectoparasite of wild guppies, would lead to the
evolution of decreased resistance in their guppy hosts. As it turned out, this
experiment was one of those studies where predictions totally missed the mark,
and because of that it broadened our understanding of the evolution of
resistance to parasites in the wild.In a nutshell, theory suggests that individuals
that invest more in defence against parasites are expected to do so at the cost
of investing in other fitness-enhancing traits. When parasite-induced mortality
increases in a population, those individuals that are better able to resist
infection will have a higher genetic representation in future generations. On
the flip side, when the negative effects of parasitism decrease, those
individuals that, for example, invest more in reproduction than defence will
have a competitive advantage over resistant individuals. A number of elegant
laboratory experiments support these predictions, but these mostly focus on “simple”
organisms (typically bacteria and protozoans, although there are some important
arthropod studies).

The rain forest of Trinidad: home to guppies and their parasites
(Photo A. Hendry)

Given these clear predictions, we set out to test whether,
under the complexities of a natural environment, removal of parasites would
lead to the evolution of decreased defence to parasites in a vertebrate host
with a complex immune system. What we found was surprising. Both four and eight
generations after being released from parasitism, our female guppies had repeatedly
increased – yes, increased! – their resistance to the parasite relative to the
ancestral population (read the paper here).

This increase in resistance could have been due to various
methodological artefacts, and we thought of some biological hypotheses for the
outcome as well. We ruled out methodological artefacts such as differences among
populations in mortality (it was not the case that less-resistant individuals
died earlier, albeit with less parasites, than more-resistant individuals) or
size (it was not the case that that the ancestral individuals were larger and
thus provided more resources for a larger parasite load which would have made
them appear to be less resistant). Among the biological explanations that we
discarded was the possibility that we were actually seeing the effects of selection
for tolerance, not for resistance. In the parasite literature, resistance
refers to the ability of hosts to reduce the number of parasites they have,
while tolerance is the ability to reduce the damage caused by a given number of
parasites. Resistance and tolerance are expected to trade off against each
other: high resistance means that parasite numbers are low, so investing in
reducing their negative effects would be a waste of resources; high tolerance
means parasites cause little damage, so investing in reducing their number
would also be a waste of resources. If parasite removal was causing selection
for decreased tolerance, then resistance could be indirectly increasing as a
response. But we found that tolerance did not change much – if anything, it
also increased after parasite removal.

Experimental guppies, parasites and me in the lab (Photo: G. Capurro)

We present several lines of evidence that suggest that this
increase in resistance after decreasing selection from parasites is also a common
outcome in wild guppy populations. We think this has to do with one of the “interacting
factors” present in natural systems: predation. As part of the experimental
translocations our guppy populations faced a strong shift not only in parasite
pressure, but also in predation-induced mortality, since they were translocated
into sites where major predators were absent. Changes in predation have been
shown to induce rapid evolution of life-history traits in guppies, and some
life-history traits such as life expectancy are known to correlate with
resistance to parasites. In our case, it seems that release from predation and
the evolved increase in life expectancy that it brings could be pleiotropically
producing increased resistance (an idea known as the pace-of-life hypothesis).
In the wild, parasites generally don’t just disappear, so this pleiotropic
connection between lifespan and resistance would be adaptive: when predators
are present,an early death is likely and resistance to parasites is an
unnecessary luxury, so individuals might use all their resources in reproducing
as early as they can, but when early death due to predation is unlikely, low
parasite resistance might greatly reduce your fitness.

Like all good research, this study has led us to new
questions. For example, how often does the pace-of-life hypothesis apply in
other systems, and under what circumstances? And more generally, is predation
always a stronger selective force than parasitism, even for traits such as
resistance that are directly related to parasites?

Sunday, February 16, 2014

I am currently in Fukuoka, Japan, at a workshop organized by Tet Yahara, Makiko Mimura, and others that is focused on
developing a Genetic Diversity Report. The basic idea is that biodiversity
science and policy currently focuses on species and their benefits to humanity,
such as ecosystem services. This perspective misses the critical point that genetic
diversity within species is incredibly important to those species and to their
benefits to humanity.

Every day during the workshop, we have been taking the
subway from our hotel to Kyushu University and, every time, we have been saturated
with posters of five young men (boys, really) who are clearly pop stars of some
sort or other. The posters are all over the walls and hang every few meters
along the ceiling of every subway car. During each commute, we probably saw 100
posters (surely a dozen would have sufficient). But what was the message? Who
were these guys and what were we supposed to be buying? Having seen these
posters a few hundred times (so maybe a dozen posters wasn’t sufficient after all), I
started to get curious and looked for a hint on the poster – but everything was
in Japanese, except for two small words “One Direction.” Oh, I had heard of
them – the current generation’s boy band, like N’Sync or The Backstreet Boys or
New Kids on the Block of previous generations. It seems One Direction was to “perform”
soon in Fukuoka – although we couldn’t figure out the date.

One Direction (top) and No Direction (bottom). From left to right: Peter Prentis, Bruce Walsh, Andrew Hendry, George Roderick, and Peter Hollingsworth. (Photo: Chris Kettle.)

This got me to thinking. One of the key features of boy
bands (and girl bands – Spice Girls!) was that they were carefully constructed
for diversity. One boy was the sensitive type, one was the bad boy, one was the
jock, and so on. Here is how Wikipedia explains it:

Seen as important to a "boy band" group's
commercial success is the group'simage, carefully controlled by managing all aspects of
the group's dress, promotional materials (which are frequently supplied toteen magazines), and music videos. The key factor of a boy band
is being trendy. This means that the band conforms to the most recent fashion
and musical trends in the popular music scene. Typically, each member of the
group will have some distinguishing feature and be portrayed as having a
particular personality stereotype, such as "the baby," "the bad
boy," or "the shy one." While managing the portrayal of popular
musicians is as old aspopular music, the particular pigeonholing of band members is a
defining characteristic of boy and girl bands.

Our main goal as a group is to convince people, including
policy makers, who don’t normally think about genetic diversity that they should
be doing so. We came up with a list of the benefits that seemed quite clear to
us – but how to convince people who weren’t already converts? I suggest the One
Direction metaphor:

Complementarity: By carefully assembling alternative
stereotypes into the band, the manager seeks to appeal to various “diverse” segments
of teenage girldom. If all of the boys were the same (clones of each other, for
example), then presumably some girls would not be interested and the records
and concerts would make less money. The same concept applies in biodiversity. If
a diversity of phenotypes/genotypes exists in a population, then the population
might use a greater diversity of habitats and thereby increase in total
abundance. Similarly, a more diverse set of genotypes will be more resistant to
the negative effects of diseases, which can’t then evolve to specialize on any
single genotype. A great example is provided by the diversity of rice types in
Chinese agriculture increasing resistance to pathogens (Zhu et al. 2000).

Portfolio effect: The appeal of different boy stereotypes to
young record-buying and concert-going girls presumably varies through time. In
some years, bad boys might be more popular, in other years, the sensitive types
might be more popular. Or perhaps each girls goes through their own preference
arc as they get older – maybe they like the shy one at first, grow into the
cute one, and graduate to the bad boy. By having multiple types in the band,
the overall popularity of the band might remain more consistent/stable through time.
The same effect again applies to biodiversity. If a number of different types
are present in the population and those different types are differentially
susceptible to environmental conditions that vary through time, then a more diverse
group will have greater stability through time. A great example is how the
diversity of sockeye salmon populations in Bristol Bay, Alaska, buffers the
entire production of the bay (and therefore harvesting by humans) in the face
of considerable environmental variation through time (Schindler et al. 2010).

Option values: By having a diversity of boy types in a band,
managers can increase the chances that some future popularity trend will be
captured by existing membership in the band. Perhaps the shy type isn’t popular
now but it will be next year. In biodiversity science, option values can work
something the same. For instance, some types in a population might not be of
much benefit for the population (or humans) now but perhaps they will be under
future environmental change. Or perhaps certain types that aren’t obviously
useful to humans in the present will eventually become so as we better
understand their beneficial properties.

Potential for change: Related to option values – but with a
different emphasis – diversity within a band can increase the potential for
future change. Perhaps the preferences of future pre-teen girls are not well
foreseen by the current stereotypes in the band but one of the key features of
boy bands is that the producers can modify them to try to match changing trends
– and the greater diversity of types to start with the greater the chance they
can be modified into a future preferred type – and the greater the chance the
band (or parts of it) will persist into the future. (Justin Timberlake is still
here.) In biodiversity, a good example is that greater amounts of genetic
diversity in the present will allow more rapid and flexible evolutionary change
in the future, which will aid population persistence (evolutionary rescue!).

Having just closed out two days of discussion, we now have
to write this report – but how to do so? Should we write a nice glossy document
that we hand out to policy makers and publish online, or should we edit a
special issue of a journal, such as Evolutionary Applications. Either approach seems
fine to me but I think that whichever route we go, we should put One Direction
on the cover. Doing so would be certain to reach more people – and what better
way to influence policy makers than by first convincing their daughters that
genetic diversity is the way to go. By virtue of One Direction and N’Sync and
The Backstreet Boys and even the Jackson Five, they are already primed to
accept it.

Tuesday, February 11, 2014

I just returned from a short trip (my tenth) to Galapagos. New experiences during the trip prompted further speculations on a phenomenon we had earlier described:
human influences on the adaptive radiation of Darwin’s finches.

An oft-repeated mantra is that remote oceanic islands (never
connected to the mainland) are natural laboratories for studying evolution. Part
of the reason is that they tend to be simple environments, making it easier to
disentangle otherwise overly-complicated ecological and evolutionary
relationships. One way in which islands are simple is that they often
lack human populations, which contributed to the evolution of strange
forms that proved to be utterly unsuited for a life with colonizing humans. As a result, the
settlement of remote islands by humans often leads to the extinction of local
life forms. However, not all isolated populations go extinct when humans
colonize, instead they often evolve to suit the new conditions.

A spectacular male Darwin's finch.

My own foray into island life involves Darwin’s finches in
Galapagos. This work obviously follows closely from the insights and work of
Peter and Rosemary Grant, and was made possible by an impromptu postdoc I did
with Jeff Podos at UMass Amherst. In general, the adaptive radiation of Darwin’s
finches is thought to have been driven by specialization of different species
on different food types, which has led to reproductive isolation (speciation)
through assortative mating by beak size (beaks, songs, and mate preferences are
all linked) and natural selection against hybrids (which are poorly suited for
either parental diet). With respect to this last point, different “adaptive
peaks” are thought to exist in the Galapagos as a result of different food
types. For example, large-beaked species evolve to use large/hard seeds and small-beaked
species evolve to use small/soft seeds but intermediate beak sizes are rare
because intermediate seeds are rare. (I just made and posted a video illustrating this phenomenon.) Darwin’s finches thus diverge onto different
adaptive peaks and the few hybrids they produce have intermediate beaks that
lack appropriate intermediate seeds on which to feed, and therefore suffer low
survival – thus keeping the two species separate.

Yum - a native food!

Our contribution to this story has been the study of two
beak size morphs within a single species (the medium ground finch, Geospiza
fortis) on the island of Santa Cruz. We (originally Jeff Podos, Sarah Huber,
Luis De Leon, Antony Herrell, and myself) have shown that these large and small
G. fortis morphs at one site (El Garrapatero) have a bimodal beak size
distribution (many large and many small individuals with relatively few
intermediates), have different diets, manifest different feeding performances (bite
force), sing different songs, show different responses to songs, mate
assortatively (large females with large males and small females with small
males), experience disruptive selection (intermediate birds have lower
survival), and show limited gene flow (based on microsatellite DNA). Stated
plainly, these two morphs seem to be part of the way to becoming separate
species, presumably through the same mechanisms as those that drove the
radiation as whole.

The two El Garrapatero G. fortis morphs.

All of the above effects were demonstrated at a site (El
Garrapatero) that is removed from any human settlements and therefore
experiences little direct human influence (although indirect influences from introduced
species are present). What happens when these two morphs – on their way to
potentially become separate species – contact a growing human population? We were
able to explore this question in a paper published in PRSB in 2006 by obtaining long
term records (1964-2005) of G. fortis beak sizes from Academy Bay, a site
immediately adjacent to the rapidly growing town of Puerto Ayora on Santa Cruz
Island. This analysis was made possible through data collected by David Snow in
1963-1964, Hugh Ford in 1968 (data was being collected for me as I was being
born!!!), the Grants and their colleagues (1970s-1980s), and our own samples
(2004 and onward). Analysis of these data showed that the beak size bimodality currently
seen in G. fortis at El Garrapatero was also present at Academy Bay in the
1960s but not thereafter. The two morphs at Academy Bay thus seemed to have
fused together into a single hyper-variable population in concert with the dramatic
increase in human population density at that site.

That is not a native food!

We proposed in the 2006 paper that fusion of the two G.
fortis morphs at Academy Bay was the result of humans introducing food types
that were accessible by finches of all beak sizes, thus turning the separate
adaptive peaks into a long adaptive ridge spanning different beak sizes. On
such a ridge, selection against intermediate birds should disappear and their
increasing abundance should eliminate the bimodality. We provided support for
this hypothesis in a paper in Evolution in 2011 that showed how the naturally strong (confirmed
at El Garrapatero) associations between diets, beak sizes, bite forces, and
gene flow that presumably drive finch diversification had all become weaker at
Academy Bay. In short, humans were causing “reverse speciation” or “despeciation”
by turning a formerly rugged adaptive landscape with distinct fitness peaks
into a broad ridge without the gaps (fitness valleys) necessary to maintain
species distinctiveness.

Our 2011 paper.

This finding was where we left the story until recently.
This year, we (spurred mainly by Luis) took up the problem again by making more
extensive surveys in the town of Puerto Ayora to see how many finches were
using human resources. Various teams of researchers and Earth Watch volunteers
would walk through town in the mornings counting birds and determining what
they were feeding on. Although I was already suspect the outcome, I was still rather
shocked by how many finches were present in the town (more than in nature) and
their incredible use of human foods – although they still found natural foods
in vacant lots and gardens. I saw finches eating waffles, chips, plantains,
rice, corn, fruit, ice cream cones, and many other items. I thereby gained a
personal confirmation of our original intuition that finches in Puerto Ayora
(Academy Bay) had access to many food types that were usable by finches of any
beak size. Then came the real kicker – at El Garrapatero.

Dozens of finches of many species eating rice.

We have been work at El Garrapatero for 12 years now. During
that time, the site has transitioned from a difficult-to-access and rarely used
site to a very popular destination for locals and tourists. The road has been
paved and extended closer to the beach, the path to the beach has been cobbled,
buses and taxis roar up and down the road, and gaggles of kids and adults play
on the beach. My first hint of possible impacts was the appearance of
non-native fruits (passion fruit) along the roadside. I was willing to accept
that this would not have a major influence on finch evolution until recently.
In 2012, we filmed Galapagos 3D IMAX – narrated by David Attenborough (no I
didn’t meet him – but it was cool to hear him say my name on air) – at El Garrapatero. The film
crew felt that our normal site, which was away from the beach, was not very
picturesque – so they asked us to set up our nets at the beach itself. I was
initially skeptical because we had never netted therefore and I couldn’t be
sure we could get finches. However, we quickly caught lots of finches – they
even seemed more abundant than at our normal site several hundred meters
inland. And they seemed attracted to us. At one point, we were waiting to film
something and noticed about 20 finches that landed right beside our banding
station. We pointed this out to the film crew and they quickly swung their
camera boom to film the finches at close range – this became the scene that
opens the finch sequence in the film. We also saw several finches attacking the
food we had brought for lunch. I was intrigued by this from a filming
perspective but didn’t dwell on it much from the perspective of evolution. This
year, however, my opinion changed.

Team Pinzones IMAX 3D (Photo by Aspen Hendry)

A few days ago, we walked with the Earth Watch volunteers
down to the beach and came across a place where finches were everywhere. We sat
down and they swarmed us. Jeff would crinkle a chip bag and they would come
running. Then Luis would do the same in a different place and they would run
over to him, jumping up on his bag and even into his hand in hopes of getting
free handouts. Nearby, other finches of several species were fighting over some
plantains someone had left out. It seems that the beach is now an accepted
place to feed the finches. This got me to thinking that the direct human
influence at El Garrapatero is increasing dramatically and that we might – in the
near future – see impacts on the finch bimodality. In particular, we documented
disruptive selection (selection against intermediate beak sized birds) in
2004-2006 before all these human changes were so dramatic. My prediction is
that selection now will be less disruptive– and perhaps even less so in the
future as human use of the site continues to expand.

An El Garrapatero G. fortis enjoys a cracker - when it shouldn't.

Evolution is coming undone in Galapagos. Human
influences are pervasive in some places and they are expanding to new places.
This is exciting as a scientist because we can now test evolutionary hypotheses
using whole-ecosystem “experiments” – we can add humans and see how evolution
changes. But it is depressing as a nature lover because a unique set of island
life might well change dramatically. Finches will still be present, of course,
but they might no longer be so diverse – at least not in sites where human
influences are strong. Fortunately the government limits those impacts to
restricted sites, leaving much of the archipelago free of direct human impacts
(indirect effects can remain strong). This policy is reassuring because it
would be a travesty if unique forms such as the “vampire finch” on Wolf Island
were to disappear.

I will report back in another decade or so.

We were even besieged by finches during our breakfast (and they ate our chocolate bread, damn it).